Literature DB >> 19404432

Actomyosin purse strings: renewable resources that make morphogenesis robust and resilient.

Alice Rodriguez-Diaz, Yusuke Toyama, Daniel L Abravanel, John M Wiemann, Adrienne R Wells, U Serdar Tulu, Glenn S Edwards, Daniel P Kiehart.   

Abstract

Dorsal closure in Drosophila is a model system for cell sheet morphogenesis and wound healing. During closure two sheets of lateral epidermis move dorsally to close over the amnioserosa and form a continuous epidermis. Forces from the amnioserosa and actomyosin-rich, supracellular purse strings at the leading edges of these lateral epidermal sheets drive closure. Purse strings generate the largest force for closure and occur during development and wound healing throughout phylogeny. We use laser microsurgery to remove some or all of the purse strings from developing embryos. Free edges produced by surgery undergo characteristic responses as follows. Intact cells in the free edges, which previously had no purse string, recoil away from the incision and rapidly assemble new, secondary purse strings. Next, recoil slows, then pauses at a turning point. Following a brief delay, closure resumes and is powered to completion by the secondary purse strings. We confirm that the assembly of the secondary purse strings requires RhoA. We show that alpha-actinin alternates with nonmuscle myosin II along purse strings and requires nonmuscle myosin II for its localization. Together our data demonstrate that purse strings are renewable resources that contribute to the robust and resilient nature of closure.

Entities:  

Year:  2008        PMID: 19404432      PMCID: PMC2639939          DOI: 10.2976/1.2955565

Source DB:  PubMed          Journal:  HFSP J        ISSN: 1955-205X


  52 in total

Review 1.  Cutaneous wound healing.

Authors:  A J Singer; R A Clark
Journal:  N Engl J Med       Date:  1999-09-02       Impact factor: 91.245

2.  Functional analysis of Cdc42 in actin filament assembly, epithelial morphogenesis, and cell signaling during Drosophila development.

Authors:  J L Genova; S Jong; J T Camp; R G Fehon
Journal:  Dev Biol       Date:  2000-05-01       Impact factor: 3.582

Review 3.  Dynamic analysis of dorsal closure in Drosophila: from genetics to cell biology.

Authors:  Antonio Jacinto; Sarah Woolner; Paul Martin
Journal:  Dev Cell       Date:  2002-07       Impact factor: 12.270

Review 4.  The efficiency of muscle contraction.

Authors:  Nicholas P Smith; Christopher J Barclay; Denis S Loiselle
Journal:  Prog Biophys Mol Biol       Date:  2005-05       Impact factor: 3.667

5.  Stress-dependent elasticity of composite actin networks as a model for cell behavior.

Authors:  M L Gardel; F Nakamura; J Hartwig; J C Crocker; T P Stossel; D A Weitz
Journal:  Phys Rev Lett       Date:  2006-03-03       Impact factor: 9.161

Review 6.  Cell contact-dependent signaling.

Authors:  F Fagotto; B M Gumbiner
Journal:  Dev Biol       Date:  1996-12-15       Impact factor: 3.582

7.  Energy-dependent regulation of cell structure by AMP-activated protein kinase.

Authors:  Jun Hee Lee; Hyongjong Koh; Myungjin Kim; Yongsung Kim; Soo Young Lee; Roger E Karess; Sang-Hee Lee; Minho Shong; Jin-Man Kim; Jaeseob Kim; Jongkyeong Chung
Journal:  Nature       Date:  2007-05-07       Impact factor: 49.962

8.  Morphogenesis in Drosophila requires nonmuscle myosin heavy chain function.

Authors:  P E Young; A M Richman; A S Ketchum; D P Kiehart
Journal:  Genes Dev       Date:  1993-01       Impact factor: 11.361

9.  Wounding induces motility in sheets of corneal epithelial cells through loss of spatial constraints: role of heparin-binding epidermal growth factor-like growth factor signaling.

Authors:  Ethan R Block; Abigail R Matela; Nirmala SundarRaj; Erik R Iszkula; Jes K Klarlund
Journal:  J Biol Chem       Date:  2004-03-23       Impact factor: 5.157

10.  Cytoskeletal filament assembly and the control of cell spreading and function by extracellular matrix.

Authors:  D J Mooney; R Langer; D E Ingber
Journal:  J Cell Sci       Date:  1995-06       Impact factor: 5.285

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  34 in total

1.  Cell ingression and apical shape oscillations during dorsal closure in Drosophila.

Authors:  Adam Sokolow; Yusuke Toyama; Daniel P Kiehart; Glenn S Edwards
Journal:  Biophys J       Date:  2012-03-06       Impact factor: 4.033

2.  Drosophila morphogenesis: tissue force laws and the modeling of dorsal closure.

Authors:  Anita T Layton; Yusuke Toyama; Guo-Qiang Yang; Glenn S Edwards; Daniel P Kiehart; Stephanos Venakides
Journal:  HFSP J       Date:  2009-12-15

3.  Crumbs is an essential regulator of cytoskeletal dynamics and cell-cell adhesion during dorsal closure in Drosophila.

Authors:  David Flores-Benitez; Elisabeth Knust
Journal:  Elife       Date:  2015-11-06       Impact factor: 8.140

4.  The receptor tyrosine kinase Pvr promotes tissue closure by coordinating corpse removal and epidermal zippering.

Authors:  Rebecca A Garlena; Ashley L Lennox; Lewis R Baker; Trish E Parsons; Seth M Weinberg; Beth E Stronach
Journal:  Development       Date:  2015-08-20       Impact factor: 6.868

5.  Remodeling Tissue Interfaces and the Thermodynamics of Zipping during Dorsal Closure in Drosophila.

Authors:  Heng Lu; Adam Sokolow; Daniel P Kiehart; Glenn S Edwards
Journal:  Biophys J       Date:  2015-12-01       Impact factor: 4.033

Review 6.  The interplay between cell signalling and mechanics in developmental processes.

Authors:  Callie Johnson Miller; Lance A Davidson
Journal:  Nat Rev Genet       Date:  2013-10       Impact factor: 53.242

7.  Combining laser microsurgery and finite element modeling to assess cell-level epithelial mechanics.

Authors:  M Shane Hutson; J Veldhuis; Xiaoyan Ma; Holley E Lynch; P Graham Cranston; G Wayne Brodland
Journal:  Biophys J       Date:  2009-12-16       Impact factor: 4.033

8.  Cell mechanics and feedback regulation of actomyosin networks.

Authors:  Rodrigo Fernandez-Gonzalez; Jennifer A Zallen
Journal:  Sci Signal       Date:  2009-12-15       Impact factor: 8.192

Review 9.  Morphogenesis of epithelial tubes: Insights into tube formation, elongation, and elaboration.

Authors:  Deborah J Andrew; Andrew J Ewald
Journal:  Dev Biol       Date:  2009-09-22       Impact factor: 3.582

10.  Integration of contractile forces during tissue invagination.

Authors:  Adam C Martin; Michael Gelbart; Rodrigo Fernandez-Gonzalez; Matthias Kaschube; Eric F Wieschaus
Journal:  J Cell Biol       Date:  2010-03-01       Impact factor: 10.539

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